After Continents Divide: Comparative Phylogeography of Reef Fishes from the Red Sea and Indian Ocean

Journal of Biogeography (J. Biogeogr.) (2013) ORIGINAL After continents divide: comparative ARTICLE phylogeography of reef fishes from the Red Sea and Indian Ocean Joseph D. DiBattista1*, Michael L. Berumen2,3, Michelle R. Gaither4, Luiz A. Rocha4, Jeff A. Eble5, J. Howard Choat6, Matthew T. Craig7, Derek J. Skillings1 and Brian W. Bowen1 1Hawai’i Institute of Marine Biology, ABSTRACT Kane’ohe, HI, 96744, USA, 2Red Sea Aim The Red Sea is a biodiversity hotspot characterized by a unique marine Research Center, King Abdullah University of fauna and high endemism. This sea began forming c. 24 million years ago with Science and Technology, Thuwal, Saudi Arabia, 3Biology Department, Woods Hole the separation of the African and Arabian plates, and has been characterized by Oceanographic Institution, Woods Hole, MA, periods of desiccation, hypersalinity and intermittent connection to the Indian 02543, USA, 4Section of Ichthyology, Ocean. We aim to evaluate the impact of these events on the genetic architec- California Academy of Sciences, ture of the Red Sea reef fish fauna. 5 San Francisco, CA, 94118, USA, Department Location Red Sea and Western Indian Ocean. of Biology, University of West Florida, Pensacola, FL, 32514, USA, 6School of Methods We surveyed seven reef fish species from the Red Sea and adjacent Marine and Tropical Biology, James Cook Indian Ocean using mitochondrial DNA cytochrome c oxidase subunit I and University, Townsville, QLD, 4811, Australia, cytochrome b sequences. To assess genetic variation and evolutionary connec- 7Department of Marine Sciences and tivity within and between these regions, we estimated haplotype diversity (h) Environmental Studies, University of San and nucleotide diversity (p), reconstructed phylogenetic relationships among Diego, San Diego, CA, 92110, USA haplotypes, and estimated gene flow and time of population separation using Bayesian coalescent-based methodology. Results Our analyses revealed a range of scenarios from shallow population structure to diagnostic differences that indicate evolutionary partitions and possible cryptic species. Conventional molecular clocks and coalescence analyses indicated time-frames for divergence between these bodies of water ranging from 830,000 years to contemporary exchange or recent range expansion. Col- onization routes were bidirectional, with some species moving from the Indian Ocean to the Red Sea compared with expansion out of the Red Sea for other species. Main conclusions We conclude that: (1) at least some Red Sea reef fauna survived multiple salinity crises; (2) endemism is higher in the Red Sea than previously reported; and (3) the Red Sea is an evolutionary incubator, occa- sionally contributing species to the adjacent Indian Ocean. The latter two conclusions – elevated endemism and species export – indicate a need for enhanced conservation priorities for the Red Sea. *Correspondence: Joseph D. DiBattista, Keywords Hawai’i Institute of Marine Biology, PO Box 1346, Kane’ohe, HI, 96744, USA. Coalescent, cryptic speciation, dispersal, genealogical concordance, gene flow, E-mail: [email protected] mitochondrial DNA, vicariance. years ago (Ma) (i.e. late-Oligocene period) by the separation INTRODUCTION of the African and Arabian plates, the ocean environment The Red Sea is a deep (maximum depth: 2920 m) and nar- that supports coral reefs originated in the early Pleistocene row (maximum width: 350 km) body of water extending (c. 5 Ma; Siddall et al., 2003; Bosworth et al., 2005). The 2270 km from 30° N in the Gulf of Suez to 13° N in the Red Sea, which now experiences minimal freshwater inflow Gulf of Aden. Although the sea began forming c. 24 million and high rates of evaporation, is characterized by ª 2013 Blackwell Publishing Ltd http://wileyonlinelibrary.com/journal/jbi 1 doi:10.1111/jbi.12068 J. D. DiBattista et al. pronounced north-to-south gradients in salinity (42& to (Randall, 1994), 33% of crustaceans, 15% of echinoderms, 37&), sea surface temperature (winter, 20–28 °C; summer, and up to 25% of corals (Cox & Moore, 2000). Endemism 26–32 °C), and nutrient concentration (low to high) (Raitsos can be even higher for some taxa, reaching 50% in the but- et al., 2011; Ngugi et al., 2012). Oceanographic current pat- terflyfishes (Roberts et al., 1992). terns and climate in the southern Red Sea (and Gulf of Although the evolutionary processes driving high rates of Aden) are heavily influenced by the northern Indian Ocean endemism are unclear, the narrow (18 km) and shallow monsoon system (Smeed, 1997, 2004; Biton et al., 2010), (137 m) strait of the Bab al Mandab, the only connection which reverses wind circulation patterns in the boreal sum- with the Indian Ocean, is likely to have played a key role mer (Southwest Monsoon, April to October) compared to (Klausewitz, 1989). The Red Sea was repeatedly isolated dur- those in the winter (Northeast Monsoon, December to ing Pleistocene glacial cycles when the sea level lowered as March; see Fig. 1). much as 120 m; whether this was achieved through physical Despite its peripheral location relative to the Indo-Pacific, isolation or the restriction of oceanic flow associated with the Red Sea is characterized by high biodiversity, including elevated salinity and temperature remains contentious (Sid- c. 300 reef-building corals (mostly species of Acropora and dall et al., 2003; Bailey, 2009). Moreover, cold-water welling Porites; Sheppard & Sheppard, 1991; Riegl & Velimirov, up off Somalia, which precludes reef formation on the 1994) and 1078 fish species (Golani & Bogorodsky, 2010), north-east African and southern Arabian coasts, is likely to which represent key resources for coastal communities. Spe- reinforce this isolation (Smeed, 1997; Kemp, 1998, 2000). cies richness appears to be highest in the central Red Sea, Some authors believe that the Bab al Mandab no longer acts with marked decreases in species abundance and changes in as a physical barrier to dispersal but that an ecological bar- species composition away from this area (DeVantier et al., rier lies within the Red Sea (Ormond & Edwards, 1987). 2000). The Red Sea also harbours one of the highest degrees Roberts et al. (1992) suggested that a turbid-water region of endemism for marine organisms, making up 14% of fishes south of 20° N in the Red Sea may limit larval dispersal, a (a) (b) 23.5ºN Thuwal (a-g) Al Lith (a-g) Oman (b) WICC (c) SC SMC NEC (d) 0º SECC Seychelles (a-f) Diego Garcia (a-g) EACC (e) SEC 23.5ºS (f) (g) Sodwana Bay (e) Figure 1 Scaled map indicating collection sites for all seven reef fish species (a, Acanthurus nigrofuscus;b,Cephalopholis argus;c, Chaetodon auriga;d,Halichoeres hortulanus;e,Lutjanus kasmira;f,Neoniphon sammara;g,Pygoplites diacanthus) sampled in the Red Sea and the Western Indian Ocean. Black lines with arrows show the major current systems flowing through each body of water (abbreviations: EACC, East African Countercurrent; NEC, Northwest Monsoon Current; SC, Somali Current; SEC, South Equatorial Current; SECC, South Equatorial Countercurrent; SMC, Southwest Monsoon Current; WICC, Western Indian Coastal Current). Note the reversing circulation of the SC (from northward to southward), the SMC (from westward to the eastward NEC), the WICC (from eastward to westward), and the current flowing into the Red Sea from the Gulf of Aden (compared with out of the Red Sea and into the Gulf of Aden) during the Northeast Monsoon season (December to March). Site-specific samples sizes are provided in Table 1. (Photo credits: M.L. Berumen, S. Moldzio and L.A. Rocha.) 2 Journal of Biogeography ª 2013 Blackwell Publishing Ltd Phylogeography of Red Sea reef fishes hypothesis which is supported by the presence of a number thereby illuminate evolutionary processes that are the well- of species in the northern/central Red Sea and the Gulf of spring of Red Sea biodiversity. Aden (just outside the Red Sea) that are absent from the southern Red Sea. MATERIALS AND METHODS Despite being acknowledged as a biodiversity hotspot for coral reef fishes based on research dating back more than Sample collection 200 years (e.g. Forsskal, 1775), little work has been con- ducted in the Red Sea using modern genetic techniques. Reef fish were collected while SCUBA diving or snorkelling Studies in this region tend to focus on the biogeography and at depths of 1–40 m between 2002 and 2011 (Fig. 1, community structure of the more iconic (and endemic) Table 1). Seven reef fish species were targeted: the brown shore fish fauna (e.g. family Chaetodontidae; Righton et al., surgeonfish, Acanthurus nigrofuscus (Forsskal, 1775); the pea- 1996). The majority of genetic studies on reef fishes have cock hind, Cephalopholis argus Schneider, 1801; the threadfin been restricted to the Gulf of Aqaba and northern Red Sea butterflyfish, Chaetodon auriga Forsskal, 1775; the checker- (Hassan et al., 2003; Kochzius & Blohm, 2005; but see board wrasse, Halichoeres hortulanus (Lacepede, 1801); the Froukh & Kochzius, 2007), and few of these considered the bluestripe snapper, Lutjanus kasmira (Forsskal, 1775); the connections between widespread taxa and other biogeograph- Sammara squirrelfish, Neoniphon sammara (Forsskal, 1775); ical provinces, particularly the Indian Ocean (Froukh & and the regal angelfish, Pygoplites diacanthus (Boddaert, Kochzius, 2008). 1772). These species were chosen because they have wide Peripheral reef habitats such as the Red Sea, which forms Indo-Pacific distributions, are abundant, represent a diversity the north-westernmost extension of the Indian Ocean, are of taxonomic families, and can be unequivocally identified typically considered to be biodiversity sinks that receive spe- in the field. Each species was sampled at two locations (Thu- cies from elsewhere but rarely export them (Briggs, 1999). wal and Al Lith) off the coast of the Kingdom of Saudi Ara- The accepted paradigm is therefore that biogeographical bia (KSA) in the central Red Sea, and at one to three sites sinks are ‘evolutionary graveyards’ that do not contribute to in the WIO (oceanic sites: Diego Garcia in the Chagos biodiversity at neighbouring sites.

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